The lipopeptide surfactin triggers induced systemic resistance and priming state responses in Arachis hypogaea L.
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Bioactive metabolites produced by multiple strains of Bacillus spp. stimulate plant defense responses. Among these, the cyclic lipopeptide surfactin was identified as an Induced Systemic Resistance (ISR) elicitor in different plant species. However, the underlying mechanisms involved in the ISR elicitation and the priming state costs in peanut plants (Arachis hypogaea L.) remain unknown. In this work, we demonstrated the ability of surfactin from B. subtilis to induce systemic resistance against Sclerotium rolfsii in peanut plants, and showed that this response involves key characteristics of priming-mediated resistance defense. Application of surfactin significantly reduced S. rolfsii disease incidence and severity on peanut plants, and an increased shoot and root dry weight was observed in surfactin pre-treated and pathogen challenged plants compared to non-treated challenged plants. In addition, peroxidase activity and phenolic compounds deposition underneath the fungal infection zone were significantly higher in surfactin pre-treated and challenged plants than in non-surfactin treated challenged plants. Collectively, results from this work indicate that ISR activity elicited by surfactin involves a priming defense state with low fitness-related costs, providing an enhanced protection against S. rolfsii in peanut plants.
KeywordsISR Defense response Priming Peanut Surfactin
This study was financially supported SECyT-UNRC, CONICET and ANPCyT.
Johan Stiben Rodriguez Melo is recipient of scholarship from FONCyT.
María Soledad Figueredo is recipient of scholarship from CONICET.
María Laura Tonelli, Fernando Ibáñez and Adriana Fabra are members of the Research Career from CONICET.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Informed consent was obtained from all individual participants included in the study.
- Ainsworth, E. A., & Gillespie, K. M. (2007). Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nat Protoc, 2(4), 875–877. https://doi.org/10.1038/nprot.2007.102.
- Babar, M. M., Khan, S. F., Zargaham, M. K., Zaidi, N.-u.-S. S., & Gul, A. (2016). Plant-Microbe Interactions: A Molecular Approach. In K. R. Hakeem & M. S. Akhtar (Eds.), Plant, Soil and Microbes: Volume 2: Mechanisms and Molecular Interactions (pp. 1–22). Cham: Springer International Publishing.Google Scholar
- Cawoy, H., Mariutto, M., Henry, G., Fisher, C., Vasilyeva, N., Thonart, P., Dommes, J., & Ongena, M. (2014). Plant defense stimulation by natural isolates of bacillus depends on efficient surfactin production. Molecular Plant-Microbe Interactions, 27(2), 87–100. https://doi.org/10.1094/mpmi-09-13-0262-r.CrossRefGoogle Scholar
- Cle, C., Hill, L. M., Niggeweg, R., Martin, C. R., Guisez, Y., Prinsen, E., et al. (2008). Modulation of chlorogenic acid biosynthesis in Solanum lycopersicum; consequences for phenolic accumulation and UV-tolerance. Phytochemistry, 69(11), 2149–2156. https://doi.org/10.1016/j.phytochem.2008.04.024.CrossRefGoogle Scholar
- Conrath, U., Beckers, G. J., Langenbach, C. J., & Jaskiewicz, M. R. (2015). Priming for enhanced defense. Annual Review of Phytopathology, 53, 97–119. https://doi.org/10.1146/annurev-phyto-080614-120132.CrossRefGoogle Scholar
- De Vleesschauwer, D., & Höfte, M. (2009). Chapter 6 Rhizobacteria-induced systemic resistance. In Advances in Botanical Research (Vol. 51, pp. 223–281): Academic Press.Google Scholar
- Figueredo, M. S., Tonelli, M. L., Ibáñez, F., Morla, F., Cerioni, G., del Carmen Tordable, M., et al. (2017). Induced systemic resistance and symbiotic performance of peanut plants challenged with fungal pathogens and co-inoculated with the biocontrol agent Bacillus sp. CHEP5 and Bradyrhizobium sp. SEMIA6144. Microbiological Research, 197(Supplement C), 65–73. https://doi.org/10.1016/j.micres.2017.01.002.CrossRefGoogle Scholar
- Hilker, M., Schwachtje, J., Baier, M., Balazadeh, S., Baurle, I., Geiselhardt, S., et al. (2016). Priming and memory of stress responses in organisms lacking a nervous system. Biological Reviews of the Cambridge Philosophical Society, 91(4), 1118–1133. https://doi.org/10.1111/brv.12215. CrossRefGoogle Scholar
- Hoagland, D. R., & Arnon, D. I. (1950). The water culture method for growing plants without soil. California Agricultural Experiment Station Circulation, 347, 31.Google Scholar
- Jourdan, E., Henry, G., Duby, F., Dommes, J., Barthelemy, J. P., Thonart, P., et al. (2009). Insights into the defense-related events occurring in plant cells following perception of surfactin-type lipopeptide from Bacillus subtilis. Molecular Plant-Microbe Interactions, 22(4), 456–468. https://doi.org/10.1094/mpmi-22-4-0456.CrossRefGoogle Scholar
- Koc, E., & Ustun, A. S. (2011). Differential induction of phenylalanine ammonia lyase and phenolics in peppers (Capsicum annuum) in response to inoculation with Phytophthora capsici. International Journal of Agriculture and Biology, 13(6), 881–887.Google Scholar
- Lugtenberg, B., & Kamilova, F. (2009). Plant-growth-promoting rhizobacteria. Annual Review of Microbiology, 63, 541–556. https://doi.org/10.1146/annurev.micro.62.081307.162918.CrossRefGoogle Scholar
- Mariutto, M., & Ongena, M. (2015). Chapter two - molecular patterns of Rhizobacteria involved in plant immunity elicitation. In H. Bais, & J. Sherrier (Eds.), Advances in Botanical Research (Vol. 75, pp. 21–56): Academic Press.Google Scholar
- Mauch-Mani, B., Baccelli, I., Luna, E., & Flors, V. (2017). Defense priming: An adaptive part of induced resistance. Annual Review of Plant Biology, 68, 485–512. https://doi.org/10.1146/annurev-arplant-042916-041132.CrossRefGoogle Scholar
- Mikulic-Petkovsek, M., Schmitzer, V., Slatnar, A., Weber, N., Veberic, R., Stampar, F., Munda, A., & Koron, D. (2013). Alteration of the content of primary and secondary metabolites in strawberry fruit by Colletotrichum nymphaeae infection. Journal of Agricultural and Food Chemistry, 61(25), 5987–5995. https://doi.org/10.1021/jf402105g.CrossRefGoogle Scholar
- Niranjan Raj, S., Lavanya, S. N., Amruthesh, K. N., Niranjana, S. R., Reddy, M. S., & Shetty, H. S. (2012). Histo-chemical changes induced by PGPR during induction of resistance in pearl millet against downy mildew disease. Biological Control, 60(2), 90–102. https://doi.org/10.1016/j.biocontrol.2011.10.011.CrossRefGoogle Scholar
- Ongena, M., Jourdan, E., Adam, A., Paquot, M., Brans, A., Joris, B., Arpigny, J. L., & Thonart, P. (2007). Surfactin and fengycin lipopeptides of Bacillus subtilis as elicitors of induced systemic resistance in plants. Environmental Microbiology, 9(4), 1084–1090. https://doi.org/10.1111/j.1462-2920.2006.01202.x.CrossRefGoogle Scholar
- Pieterse, C. M., Zamioudis, C., Berendsen, R. L., Weller, D. M., Van Wees, S. C., & Bakker, P. A. (2014). Induced systemic resistance by beneficial microbes. Annual Review of Phytopathology, 52, 347–375. https://doi.org/10.1146/annurev-phyto-082712-102340.CrossRefGoogle Scholar
- Sosa Alderete, L. G., Talano, M. A., Ibanez, S. G., Purro, S., Agostini, E., Milrad, S. R., et al. (2009). Establishment of transgenic tobacco hairy roots expressing basic peroxidases and its application for phenol removal. Journal of Biotechnology, 139(4), 273–279. https://doi.org/10.1016/j.jbiotec.2008.11.008.CrossRefGoogle Scholar